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PMID: 12660155 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional expression of the epithelial Ca(2+) channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex.

The EMBO journal ·Vol. 22 ·No. 7 ·2003-04-01 ·Pages 1478-87

van de Graaf SF, Hoenderop JG, Gkika D, Lamers D, Prenen J, Rescher U, Gerke V, Staub O, Nilius B, Bindels RJ

Abstract

TRPV5 and TRPV6 constitute the Ca(2+) influx pathway in a variety of epithelial cells. Here, we identified S100A10 as the first auxiliary protein of these epithelial Ca(2+) channels using yeast two-hybrid and GST pull-down assays. This S100 protein forms a heterotetrameric complex with annexin 2 and associates specifically with the conserved sequence VATTV located in the C-terminal tail of TRPV5 and TRPV6. Of these five amino acids, the first threonine plays a crucial role since the corresponding mutants (TRPV5 T599A and TRPV6 T600A) exhibited a diminished capacity to bind S100A10, were redistributed to a subplasma membrane area and did not display channel activity. Using GST pull-down and co-immunoprecipitation assays we demonstrated that annexin 2 is part of the TRPV5-S100A10 complex. Furthermore, the S100A10-annexin 2 pair colocalizes with the Ca(2+) channels in TRPV5-expressing renal tubules and TRPV6-expressing duodenal cells. Importantly, downregulation of annexin 2 using annexin 2-specific small interfering RNA inhibited TRPV5 and TRPV6-mediated currents in transfected HEK293 cells. In conclusion, the S100A10-annexin 2 complex plays a crucial role in routing of TRPV5 and TRPV6 to plasma membrane.

MeSH Terms
Animals Annexin A2/metabolism Base Sequence Calcitriol/metabolism Calcium Channels/metabolism Calcium-Binding Proteins/metabolism DNA Primers Epithelium/metabolism Gene Silencing Immunohistochemistry Mice Protein Binding RNA Interference Reverse Transcriptase Polymerase Chain Reaction S100 Proteins Two-Hybrid System Techniques
Chemicals
Annexin A2 Calcium Channels Calcium-Binding Proteins DNA Primers S100 Proteins S100 calcium binding protein A10 Calcitriol
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
van de Graaf Stan F J
Department of Cell Physiology, Nijmegen Center for Molecular Life Sciences, University Medical Center Nijmegen, PO Box 9101, NL-6500 HB Nijmegen, The Netherlands.
Hoenderop Joost G J
Gkika Dimitra
Lamers Dennis
Prenen Jean
Rescher Ursula
Gerke Volker
Staub Olivier
Nilius Bernd
Bindels René J M
References (44)
44 references, click to expand
  1. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit.
    Genes Dev. 1993 Apr;7(4):555-69 PMID: 8384581
  2. Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption.
    J Biol Chem. 1999 Aug 6;274(32):22739-46 PMID: 10428857
  3. Cloning and functional expression of rat CLC-5, a chloride channel related to kidney disease.
    J Biol Chem. 1995 Dec 29;270(52):31172-7 PMID: 8537381
  4. Annexin II up-regulates cellular levels of p11 protein by a post-translational mechanisms.
    Biochem J. 1996 Jan 1;313 ( Pt 1):51-5 PMID: 8546709
  5. Increased content of annexin II (p36) and p11 in human placenta brush-border membrane vesicles during syncytiotrophoblast maturation and differentiation.
    Placenta. 1996 Nov;17(8):669-76 PMID: 8916217
  6. Permeation and gating properties of the novel epithelial Ca(2+) channel.
    J Biol Chem. 2000 Feb 11;275(6):3963-9 PMID: 10660551
  7. Localization of the epithelial Ca(2+) channel in rabbit kidney and intestine.
    J Am Soc Nephrol. 2000 Jul;11(7):1171-8 PMID: 10864572
  8. TRP and the PDZ protein, INAD, form the core complex required for retention of the signalplex in Drosophila photoreceptor cells.
    J Cell Biol. 2000 Sep 18;150(6):1411-22 PMID: 10995445
  9. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor.
    Cell. 2000 Oct 27;103(3):525-35 PMID: 11081638
  10. Modulation of the epithelial calcium channel, ECaC, by intracellular Ca2+.
    Cell Calcium. 2001 Jun;29(6):417-28 PMID: 11352507
  11. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  12. Expression of CaT-like, a novel calcium-selective channel, correlates with the malignancy of prostate cancer.
    J Biol Chem. 2001 Jun 1;276(22):19461-8 PMID: 11278579
  13. Calcitriol controls the epithelial calcium channel in kidney.
    J Am Soc Nephrol. 2001 Jul;12(7):1342-9 PMID: 11423563
  14. Complex formation and submembranous localization of annexin 2 and S100A10 in live HepG2 cells.
    FEBS Lett. 2001 Jul 6;500(3):137-40 PMID: 11445072
  15. Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9742-7 PMID: 11481446
  16. Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects.
    Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13324-9 PMID: 11687634
  17. Distribution of transcellular calcium and sodium transport pathways along mouse distal nephron.
    Am J Physiol Renal Physiol. 2001 Dec;281(6):F1021-7 PMID: 11704552
  18. Function and expression of the epithelial Ca(2+) channel family: comparison of mammalian ECaC1 and 2.
    J Physiol. 2001 Dec 15;537(Pt 3):747-61 PMID: 11744752
  19. Molecular mechanism of active Ca2+ reabsorption in the distal nephron.
    Annu Rev Physiol. 2002;64:529-49 PMID: 11826278
  20. A unified nomenclature for the superfamily of TRP cation channels.
    Mol Cell. 2002 Feb;9(2):229-31 PMID: 11864597
  21. p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1.
    EMBO J. 2002 Sep 2;21(17):4439-48 PMID: 12198146
  22. Modulation of renal Ca2+ transport protein genes by dietary Ca2+ and 1,25-dihydroxyvitamin D3 in 25-hydroxyvitamin D3-1alpha-hydroxylase knockout mice.
    FASEB J. 2002 Sep;16(11):1398-406 PMID: 12205031
  23. Homo- and heterotetrameric architecture of the epithelial Ca2+ channels TRPV5 and TRPV6.
    EMBO J. 2003 Feb 17;22(4):776-85 PMID: 12574114
  24. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs.
    Nucleic Acids Res. 1984 Sep 25;12(18):7057-70 PMID: 6207484
  25. The regulatory chain in the p36-kd substrate complex of viral tyrosine-specific protein kinases is related in sequence to the S-100 protein of glial cells.
    EMBO J. 1985 Nov;4(11):2917-20 PMID: 2998764
  26. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli.
    Gene. 1987;57(2-3):267-72 PMID: 3319781
  27. A role for calpactin in calcium-dependent exocytosis in adrenal chromaffin cells.
    Nature. 1989 Jul 27;340(6231):313-5 PMID: 2526299
  28. The tight association of the tyrosine kinase substrate annexin II with the submembranous cytoskeleton depends on intact p11- and Ca(2+)-binding sites.
    J Cell Sci. 1992 Nov;103 ( Pt 3):733-42 PMID: 1478969
  29. The TRP channels, a remarkably functional family.
    Cell. 2002 Mar 8;108(5):595-8 PMID: 11893331
  30. Annexins: from structure to function.
    Physiol Rev. 2002 Apr;82(2):331-71 PMID: 11917092
  31. Expression of the novel epithelial Ca2+ channel ECaC1 in rat pancreatic islets.
    J Histochem Cytochem. 2002 Jun;50(6):789-98 PMID: 12019295
  32. Annexin II light chain regulates sensory neuron-specific sodium channel expression.
    Nature. 2002 Jun 6;417(6889):653-6 PMID: 12050667
  33. 1,25-dihydroxyvitamin D(3)-independent stimulatory effect of estrogen on the expression of ECaC1 in the kidney.
    J Am Soc Nephrol. 2002 Aug;13(8):2102-9 PMID: 12138142
  34. Fast and slow inactivation kinetics of the Ca2+ channels ECaC1 and ECaC2 (TRPV5 and TRPV6). Role of the intracellular loop located between transmembrane segments 2 and 3.
    J Biol Chem. 2002 Aug 23;277(34):30852-8 PMID: 12077127
  35. Annexin II modulates volume-activated chloride currents in vascular endothelial cells.
    J Biol Chem. 1996 Nov 29;271(48):30631-6 PMID: 8940038
  36. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains.
    Science. 1997 Jan 3;275(5296):73-7 PMID: 8974395
  37. Differential expression of annexins I, II and IV in human tissues: an immunohistochemical study.
    Histochem Cell Biol. 1998 Aug;110(2):137-48 PMID: 9720986
  38. Polarized localizations of annexins I, II, VI and XIII in epithelial cells of intestinal, hepatic and pancreatic tissues.
    J Cell Sci. 1998 Oct;111 ( Pt 20):3007-15 PMID: 9739074
  39. The crystal structure of a complex of p11 with the annexin II N-terminal peptide.
    Nat Struct Biol. 1999 Jan;6(1):89-95 PMID: 9886297
  40. Mutational analysis of cysteine-rich domains of the epithelium sodium channel (ENaC). Identification of cysteines essential for channel expression at the cell surface.
    J Biol Chem. 1999 Jan 29;274(5):2743-9 PMID: 9915805
  41. Molecular identification of the apical Ca2+ channel in 1, 25-dihydroxyvitamin D3-responsive epithelia.
    J Biol Chem. 1999 Mar 26;274(13):8375-8 PMID: 10085067
  42. Annexin II increases osteoclast formation by stimulating the proliferation of osteoclast precursors in human marrow cultures.
    J Clin Invest. 1999 Jun;103(11):1605-13 PMID: 10359570
  43. The epithelial calcium channel, ECaC, is activated by hyperpolarization and regulated by cytosolic calcium.
    Biochem Biophys Res Commun. 1999 Aug 2;261(2):488-92 PMID: 10425212
  44. Mammalian Ras interacts directly with the serine/threonine kinase Raf.
    Cell. 1993 Jul 16;74(1):205-14 PMID: 8334704
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2003-04-01
Pages
1478-87
Language
English
Region
England
NLM ID
8208664
PMCID
PMC152906
Subset
IM
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